Download Evolution of sexuality: biology and behavior

Evolution of sexuality: biology and behavior
GREGORY G. DIMIJIAN, MD
Sexual reproduction in animals and plants is far more prevalent than
asexual reproduction, and there is no dearth of hypotheses attempting
to explain why. Even bacteria and viruses, which reproduce by cloning,
engage in promiscuous horizontal gene exchange (“parasexual reproduction”) on such short time scales that they evolve genotypic diversity
even more rapidly than eukaryotes. (We confront this daily in the form
of antimicrobial resistance.) The host-parasite and host-pathogen arms
race purports to explain the prevalence of sexual reproduction, yet there
are over a dozen other hypotheses, including the proposition that sexual
reproduction purges the genome of deleterious mutations. An equally
daunting challenge is to understand, in terms of evolutionary logic, the
C
hildren learn that most plants and animals reproduce
sexually and come in two sexes. They also learn that
many plants and a few animals have both sexual organs
in the same body (hermaphrodites) yet still reproduce with two
distinct kinds of gametes, eggs and sperm. They also learn that
sexual reproduction is much more common than asexual.
It is critical to distinguish between natural selection and
sexual selection, whenever this is possible. The psychologist
Geoffrey Miller stated: “Natural selection is about living long enough
to reproduce; sexual selection is about convincing others to mate with
you.” This is an excellent comparison in a nutshell, even though
it leaves out male-male competition. The Table compares natural
and sexual selection.
Before looking at hypotheses about the ubiquity of sexuality, I’d like to describe some of the extraordinary ways the two
sexes differ in form and behavior, especially during courtship
and mating. I’ll stick to nonhuman animals in this article and
venture into the more controversial waters of human behavior
in a future article.
SEXUAL SELECTION: EXAMPLES OF SEXUAL DIMORPHISM AND
MALE-MALE COMPETITION
When we observe animals in nature or pets in our homes, do
we see a difference in form or behavior between the sexes? I am
referring to more than just the anatomy of their reproductive
organs. Is there a difference in size, color, ornaments, or behavior between the sexes of the same species of animal? More often
than not, the answer is a resounding yes. The difference is called
“sexual dimorphism.”
Birds provide a striking example of sexual dimorphism. In
many species the male is more colorful or ornamented than the
female (Figure 1) and is the one who sings, displays, and chases
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jungle of diverse courtship and mating strategies that we find in nature.
The phenotypic plasticity of sex determination in animals suggests that
the central nervous system and reproductive tract may not reach the same
endpoint on the continuum between our stereotypic male and female extremes. Why are there only two kinds of gametes in most eukaryotes? Why
are most flowering plants, and few animals, hermaphroditic? Why do male
animals compete more for access to females than the other way around in
most animals that have been studied? This review presents more questions
than answers, but an extraordinary wealth of data has been collected, and
new genetic techniques will provide new answers. The possible relevance
of these data to human sexuality will be discussed in a future article.
Table. Comparison of natural and sexual selection
Natural selection
Genes conferring protection against pathogens and parasites, or against
immune systems, and coding for changes that adapt their bearers to
changed environmental conditions should achieve better representation
in future generations, assuming a variety of genes can become more
common in the gene pool of a species at the expense of others. There is
a good analogy with human selection in the domestication of animals,
plants, and microorganisms, except for the “artifact” of human cognitive choice.
Sexual selection
Female choice (less commonly male choice): One sex (the one with greater
parental investment) is more choosy, and the other sex competes more
intensely for access to that sex.
Male-male competition (less commonly female-female competition): The
more competitive sex may become larger and may evolve more showy
ornaments or weaponry.
away other males. It is surprising that the huge peacock tail is
compatible with survival in the wild (Figures 2 and 3), as the
male is encumbered with a monstrous burden of feathers and is
surely handicapped if attacked by a predator. Such baggage could
hardly evolve by natural selection, as it would be a handicap,
not a survival advantage. The color and displays of males also
render them more visible to predators. So how could such handiFrom the Department of Psychiatry, The University of Texas Southwestern Medical
Center at Dallas, Dallas, Texas.
Corresponding author: Gregory G. Dimijian, MD (e-mail: [email protected]).
All photographs by Greg and Mary Beth Dimijian (website: dimijianimages.com).
BUMC PROCEEDINGS 2005;18:244–258
a
b
Figure 1. (a) Male Resplendent Quetzal in nest hole in Costa Rica, his long tail still pointing the way it did when he entered. The long tail and bright
colors of many male birds are examples of female choice, a form of sexual selection, distinct from natural selection, even though it is still “natural.”
The ornaments and colors of such male birds are actually survival handicaps, and research has shown that choice of such mates by females increases
their reproductive success by providing them with robust genes and the likelihood that their male offspring will also be more attractive to females.
(b) Female Resplendent Quetzal in Costa Rica, with a much shorter tail than the male and less bright colors.
Online distribution of illustration is prohibited.
See printed journal.
Figure 2. Peacock with a highly ornamented tail which, like the male quetzal’s tail, evolved by female
choice. If some “eyes” are removed from his tail, he becomes less attractive to peahens. It is hard to
imagine how such an enormous encumbrance would be compatible with escape from predators, and
indeed further enlargement of the tail may have been constrained by natural selection.
caps evolve? The answer is by female choice, one kind of sexual
selection in which one sex prefers to mate with a partner having
a particular trait or resource. Sexual selection is not the same
as natural selection, even though it is “natural.” It can even be
antagonistic to natural selection; if it goes too far, it is countered
by natural selection, in some cases because males become vulnerable to predators.
Sexual selection is a little-appreciated but critically important
evolutionary mechanism, moving certain alleles preferentially
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Figure 3. Gary Larson got this one right!
into the future just as natural selection does. Females who choose
showy mates have showy male offspring, who will in turn be more
attractive to females in the future, so genes that promote the
preference are passed on.
Experimental support for the evolutionary advantages of
female choice is abundant and well accepted. In one study, the
long tails of male widowbirds in Africa were trimmed, and the
removed portions were glued onto those of other males, making
their tails abnormally long. Those males had the highest mating
EVOLUTION OF SEXUALITY: BIOLOGY AND BEHAVIOR
245
Figure 6. Adult male impalas clash in deadly earnest in competition for females
and territory, in the Okavango Delta of Botswana, southern Africa.
Figure 4. Young male giraffes in East Africa gently spar for as long as an hour, in
preparation for more serious sparring as adults in competition for females. The
head and neck are also used as powerful weapons in killing predators.
Figure 7. Male elk with his harem in Yellowstone National Park. His antlers and
larger size result from male-male competition, a form of sexual selection.
Figure 5. Young male Australian sea lions confront each other in
practice bouts of sparring, in preparation for competition for females
as adults. Male-male competition is one form of sexual selection and
often results in males being larger than females and having more
formidable weaponry.
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success, and the males with short tails had the lowest success.
Peacocks with eyes trimmed from their tails have the least mating
success. Roosters with large bright combs are the most attractive
to females. Male swordtail fish with the longest tails or brightest
tail coloration are the most attractive to females. The brightest
and most ornamented male birds, or those with territory, are the
most attractive to females. Tungara frogs with the loudest calls
attract the most females. Female crickets prefer males whose
songs have the greatest complexity. In most cases the choices
made by females are sound in an evolutionary sense, in that the
males they choose have the greatest freedom from parasites and
greatest fitness. Female choice is usually not arbitrary but based
on genetically determined preferences for traits in males that are
“badges” of quality genes.
Sexual selection is not just about female choice but also
about male-male competition (Figures 4–6), which may result
in the evolution of males that are much larger than females and
endowed with weaponry. Elephant tusks and deer antlers are
larger in males and confer greater competitive ability on their
owners; in some cases female choice may also contribute to a
male’s weaponry. In the case of elk, sea lions, and gorillas, the
strongest male gains a harem by male-male competition (Figure
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Figure 9. A lioness licks her newborn cubs that were just delivered in a protected
place away from the pride, probably for the safety of the cubs in the case of takeover by a new male coalition. Females tend to coordinate their pregnancies, and
when their cubs are returned to the pride they are suckled by all lactating females.
Lions are the only highly “social” cat; other cats around the world are solitary as
adults, except for cheetah brothers, which may remain together.
Figure 8. Lions mating in the Masai Mara of Kenya, with the male’s grimace
and female’s reaction at the moment of ejaculation. The female mates
with many males before “committing” her eggs to fertilization. When she
accepts a male, they often copulate every 15 minutes for 3 days and nights,
the male never letting her wander more than a few feet away. Infanticide
by new males that take over a pride may help explain her delay in ovulating, as she may be testing the stability of her pride’s male coalition.
7). Any alleles that contribute to his greater strength and size
are passed on to his male offspring. The weaponry may exact a
high cost to the bearer; Irish elk from the Siberian Arctic became
extinct about 7700 years ago, and it is estimated that the huge
antlers of the male contained up to 16 pounds of calcium and 8
pounds of phosphate, a high nutritional price to pay as antlers
are regrown every year.
Natural selection, in contrast, fine-tunes adaptations of both
sexes to the dynamic changes that occur constantly in the biotic
and abiotic environment, such as changing virulence of pathogens and parasites, changing relationships between mutualists,
changing immune system challenges to pathogens, changing
climate, and changing food availability. The latest mass extinction, caused by humans, is occurring at such a breakneck pace
that evolutionary change can’t keep up, except perhaps in microorganisms.
A remarkable study of both natural and sexual selection operating simultaneously describes an “antiaphrodisiac” chemical
deposited on a female moth by the male who mates with her (1).
The chemical, benzyl cyanide, repels other male moths, serving
as a kind of chastity belt and increasing the male’s certainty of
paternity. This is not a conscious activity on his part, of course,
but simply a programmed behavior brought about by genes that
are favored by sexual selection—in this case, male-male compeJULY 2005
tition. All else being equal, his genes may outcompete those of
males whose genes don’t promote the behavior. But there is a
catch: a tiny parasitic wasp has learned to home in on the smell
of the chemical and hitches a ride on the mated female to the
place where she will lay her eggs. The female wasp then injects
her own eggs into the larger moth eggs, which serve as food for
her offspring. The “antiaphrodisiac” chemical, then, repels other
male moths but inadvertently dooms his genetic contribution.
We are seeing natural selection constraining sexual selection,
with a kind of selection arms race going on. If this strategy is
widespread in nature, it could constrain the evolution of sexual
communication between hosts, as parasites learn to home in on
host pheromones.
Lionesses in East Africa mate with many males, including
males outside of their pride, before ovulating. In effect, they delay ovulation for a month or longer after inviting males to mate
(Figure 8). Infanticide by a coalition of takeover males is common
in lion prides. Mating females may be delaying “commitment” of
their eggs until they are more confident that their pride males are
strong enough to resist invasion and takeover by itinerant males,
because replacement means that any newborn cubs are likely to be
killed by the takeover males (Figure 9). The females are of course
not doing this consciously but with behavioral predispositions
imposed by genes that survive preferentially over other genes
because they promote greater reproductive success.
Lions are the only highly “social” cat, forming prides in which
females are permanent members and male “coalitions” come and
go. All other cats are solitary as adults, except perhaps cheetahs.
Cheetah brothers sometimes remain together as adults.
Infanticide by males is a significant source of infant mortality
in mammals. In primates it has been found in 35 different species
(2). It is clearly an example of male-male competition (one form
of sexual selection) with a gain only to the takeover males and a
loss to the females and the social group.
Why are chimpanzee testes four times the size of gorilla testes,
even though male chimpanzees are one fourth the size of male
gorillas? The likely explanation is that male gorillas keep harems,
EVOLUTION OF SEXUALITY: BIOLOGY AND BEHAVIOR
247
Figure 10. “Pregnant” male seahorse, carrying his young in an abdominal pouch.
His certainty of paternity is absolute, as the female injects her eggs into his pouch,
where he fertilizes them. In some male seahorses there is a placenta-like structure
for nourishing the young. His sperm count is low, as is predicted by evolutionary
theory in the face of absent sperm competition with other males.
and sperm quantity is not important as a form of male-male competition, whereas female chimpanzees mate promiscuously and
the larger the male’s sperm volume, the more likely his success
in impregnating a female who has mated (or will mate) with
other males.
Some male seahorses carry their young in an abdominal pouch
into which the female injects her eggs (Figure 10). He fertilizes
them there, certain of his paternity, and—like gorillas—enjoys
low sperm competition and has a relatively low sperm count. I
will say more about seahorses later in this article.
Male-male competition may go to extremes. A recent study
of the giant Australian cuttlefish (a kind of squid) describes the
behavior of small “sneaker males” that swim into the danger zone
of other larger males courting females and rapidly mimic the appearance and behavior of females (squids and octopuses are master
quick-change artists when it comes to color and pattern change).
When his disguise works, he is tolerated long enough for him to
inseminate the female and quickly make his escape (3).
Male-male competition has a more sacrificial side. Males of
some cannibalistic spiders and insects allow the female to eat
them after mating. The male yellow garden spider, Argiope aurantia, has been shown to collaborate in his own instantaneous
death: he dies by his own “decision” after inserting the second of
his two pedipalps (mating appendages) inside one of the female’s
genital apertures. He becomes unresponsive, and his heartbeat
ceases within minutes of insertion. His body may thus serve as
a mating plug, a kind of temporary chastity belt that delays or
prevents other males from taking their turn. His genes, which
program the behavior, carry the day. Their ephemeral creation,
his body, is merely a vehicle (Figure 11) (4).
THE BEWILDERING VARIETY OF REPRODUCTIVE STRATEGIES IN
NATURE
The movie Finding Nemo has made the orange clownfish a lovable and popular fish, living on coral reefs in the protected shelter
of its anemone. In each clownfish “family,” the female is largest,
the male second largest, and nonbreeders smaller (Figure 12). If
the female dies, the male changes sex and becomes the breeding
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Figure 11. A female Argiope garden spider on her web in North
Texas, with a zig-zag structure called the stabilimentum, the function of which is unknown. The male is a tiny fraction of her size,
and after inserting his mating appendage into her genital aperture
he dies spontaneously, of his own accord, remaining in place. One
hypothesis is that he thus serves as a mating plug, a kind of chastity
belt, temporarily blocking any other male from taking his turn.
Figure 12. Orange clownfish share a protective anemone on a Philippine coral reef.
The female is largest and the male second largest. If the female dies, the male
changes sex and takes her place, and the largest nonbreeder becomes the breeding
male. Subordinates in the group queue for breeding positions.
female, and the largest nonbreeder becomes the breeding male
(5). In fish that can change sex, both male and female gonads are
present but only one is active at any time; the social environment
can switch the gender of an individual by turning some genes on
and others off, activating one gonad and suppressing the other,
with gender-appropriate behavior following the change.
True hermaphroditism, on the other hand, involves both male
and female reproductive tracts remaining functional simultane-
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VOLUME 18, NUMBER 3
ously in the same individual. Sea hares are hermaphroditic mollusks that look like snails without a shell; they are male in front
and female behind. They form daisy chains on the ocean floor,
with a dozen or more individuals copulating fore and aft; they
sometimes form a closed circle!
In hermaphroditic bass, one individual releases sperm and
the other eggs, then they reverse roles and release gametes again.
In this way they achieve mutual outcrossing. Is this not more efficient than the assignment of one sex to one individual? Surely
it is, but no one knows why it is not more universal.
Teleost fishes (most bony fishes, the largest class of vertebrates) range in sexual phenotypes from species with permanent
sexes, such as cichlids, to species that change sex once in their
lives and to those that change sex multiple times. “Sequential
hermaphrodites” alternate between donating sperm and eggs
without permanent commitment to the male or female gender.
Others reproduce first as males and then switch permanently
to the female sex, and others do it the other way around. Some
fish have two distinct male phenotypes: one, usually larger, that
guards a female, and a second type, usually smaller, that moves
into the other male’s space and “sneaks” a quick copulation with
the female. Fertilization is external in most fish species.
Parental care shows great diversity in fishes. Some provide
none at all, like Atlantic herring, which form huge schools of
both sexes and freely shed their eggs and sperm (milt) into the
water and then leave. Other fishes build nests and care for both
the eggs and newly hatched young. Others carry the fertilized
eggs with them, often in their mouths but also in gill cavities or
in special pouches on the body (seahorses and pipefishes).
Deep-sea anglerfish have such a bizarre reproductive strategy
that it was difficult to discover. At their low population densities
in the deep sea, it is hard for them to find mates. In some species,
when the much smaller male finds a female, he attaches himself to
her and the dermis of his snout and lower jaw becomes completely
fused to her body (6). Apparently, a continuity is established
between the female blood vascular system and that of the male,
although critical proof of this is lacking. Degenerative changes
in all organs of the male have been seen except for the relatively
large testis, which remains functional. The male thus becomes
a degenerate parasite, not much more than a male reproductive
organ attached to the female. Now with a guaranteed source of
sperm, she supports “him” nutritionally for the rest of his life.
He is in effect a xenograft that is not rejected, a challenge for an
understanding of how the immune system accommodates this
foreign tissue. One could even question whether what remains
is a female with a parasitic male or a single hermaphroditic fish.
Sperm release into the water is coordinated with her release of
eggs. Once fertilized, the eggs are buoyant and float to the surface
of the ocean. The hatchlings that survive feed on plankton until
they mature and return to deeper waters.
There are 24,500+ species of fishes, 21⁄2 times more species
than birds and 5 times more than mammals, and their bewildering variety of reproductive strategies offers limitless opportunities
for understanding how two sexes and two gamete types engage
in an arms race for future genetic representation, in the same or
different bodies. We have just begun to explore the patterns and
the evolutionary logic.
JULY 2005
The biologist Daniel Janzen commented that plants move
twice in their lives: as pollen and seed. Both moves involve reproduction. Plants have an amazing body organization that is often
forgotten: there are no gonads for producing sperm and eggs; the
body is instead modular with repetitive structures that include
totipotent stem cells capable of producing flowers with gametes
every flowering season. “Immortal” germ cells arise de novo from
somatic cells on branches and even on the trunk of some trees
(cauliflory, as in the cacao tree, the source of chocolate). The
great longevity of plants (some bristlecone pines are over 4000
years old) is made possible by this ability to maintain unspecialized
cells in the adult over long periods of time. Plants can even be
propagated from small pieces of tissue, or from single cells, because
many somatic cells remain totipotent throughout life. In contrast,
the stem cells of adult mammals, such as hematopoietic cells in the
bone marrow, can produce only a restricted spectrum of cell types
and are “pluripotent,” one step down from totipotent.
Most flowering plants (angiosperms) are hermaphroditic,
and every flower is usually bisexual, with both male and female
elements in the same flower. Oaks are hermaphroditic but have
separate male and female flowers on the same tree, as do most
gymnosperms (conifers and cycads). Most hermaphroditic plants
have mechanisms that prevent self-fertilization, avoiding inbreeding depression.
In mammals, including humans, true hermaphroditism occurs
occasionally as a genetic mistake. The causes are not understood,
but a few cases have been attributed to the movement of the Sry
gene (which triggers testis development) to a site on the X chromosome (7). Testes, ovaries, and ovotestes can occur in various
combinations. For unknown reasons, hermaphroditism in humans
is more common in Africa and the Middle East.
The evolutionary biologist Olivia Judson wrote that the battle
of the sexes is an eternal war (8). With mating strategies, she
added, the only rule is that there are no rules. True monogamy
with partner fidelity is “so rare that it is one of the most deviant
behaviors in biology.” It is rare because it rarely serves the genetic
interest of either party, let alone both.
You may argue, however, that over 90% of bird species are
monogamous, but it turns out that the monogamy is more often
“social” (i.e., lacking sexual fidelity). Both partners collaborate
in rearing the young, but more and more genetic studies show
partner infidelity during the mating period, so that males often
help raise young that are not theirs. Monogamy may also be “serial,” lasting for only one breeding season.
The Wandering Albatross provides a striking exception to
partner infidelity. This albatross is one of the most remarkable
animals in the world (Figure 13). These enormous birds, with a
wingspan that measures 11 feet, the longest of any bird (one wing
is as long as your outstretched arms), mate for life, which is often
6 decades or longer. After leaving its natal nest on a subantarctic
island such as South Georgia Island, a newly fledged bird—the size
of an adult but a darker color—takes to the air and lives on the
wing for the next 5 to 7 years, before coming to land and finding
a lifelong mate. It feeds during those years by landing briefly on
the water and catching squid, fish, and offal thrown off of fishing
boats. Albatrosses are masters of gliding skills, using their narrow, long wings to drift effortlessly on the winds surrounding the
bottom of the world.
EVOLUTION OF SEXUALITY: BIOLOGY AND BEHAVIOR
249
Figure 13. This Wandering Albatross fledgling, on its nest on South Georgia Island,
is almost ready to start an uninterrupted 5- to 7-year-long flight over the southern
ocean surrounding the bottom of the world, returning to land after all those years
to mate monogamously for life. Even at only 9 months of life, it has a wingspan of
11 feet, the longest of any bird; we were 20 feet away and it seemed like a giant.
After raising one young, the two partners depart for another
year or two of gliding over the southern waters and return to
the same place at the same time to breed again. Sadly, long-line
fishing boats with nets up to 80 miles long have killed tens of
thousands of females, who fly farther north than the males and
thus encounter more fishing boats. Males are now returning to
land to find their mate missing. They either fail to reproduce that
year or must find a younger, more inexperienced female, who may
die in a fishing net the following year.
The Rime of the Ancient Mariner, written by Samuel Taylor
Coleridge in 1797, chronicled the killing of a Wandering Albatross (a “pious bird of good omen”) as it followed a ship. The
Wandering Albatross is my favorite of all birds, and I long to see
it again effortlessly following our ship in the stormy waters of the
southern ocean.
Birds mate by approximating their cloacae, as the males of
most bird species lack a penis. The cloaca is the common outlet
of the alimentary canal, bladder, and reproductive tract, in both
sexes. A minority of birds, including ducks, geese, flamingos, and
ostriches, have a retractable grooved penis fixed to the wall of the
cloaca. The ostrich penis may reach 8 inches in length.
Amphibians (frogs, toads, salamanders) lay eggs that lack a
shell and the embryonic membranes that allow egg survival on
dry land. The moist environments in which frogs lay eggs are
endlessly varied (9). Some eggs are deposited in water, some in a
foam nest, some in burrows, and some high in trees in temporary
water pools in plants such as bromeliads. Most amphibians fertilize their eggs externally, but a few frogs are “viviparous,” the eggs
fertilized inside the female reproductive tract and little froglets
delivered after hatching. In one frog species the female swallows
the fertilized eggs and broods them in her stomach. In another
species the male broods the eggs in his mouth. Females of so-called
“marsupial” frogs brood the eggs and carry the tadpoles in a pouch
on their back. The female dart-poison frog of the Amazon simply
carries her tadpoles on her back and feeds them with unfertilized
eggs once she carries them to water in a bromeliad.
All frogs, salamanders, and newts studied to date have
separate sexes, and gender is determined by sex chromosomes.
Exposure to high incubation temperatures, however, can reverse
gonadal sex determination in some species.
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Figure 14. Standing on his hands and rolling a ball of herbivore dung with his
hind legs, a male dung beetle in East Africa courts a female in the process, who
rides along on the ball. At some point he decides to start digging, and the party
disappears slowly down the hole, to a depth of several feet. Once there the female
deposits one or more eggs in the dung, now safe from predators. Dung beetles
are unsung heroes of nutrient recycling and soil turnover in the tropics. We wear
them on our body in the form of scarab jewelry.
Dung beetles in East Africa (Figure 14) bury and recycle
enormous amounts of dung from elephants and other herbivores. Males compete fiercely for the opportunity to form and
roll away a ball of dung, in the process attracting a female who
rides passively on the rolling ball. The easiest way for a male to
obtain a ball of dung is to steal it from another beetle who has
assiduously formed it. Whoever the owner, he rolls the ball across
a long stretch of African savanna by standing on his hands and
pushing with his feet. At some point he decides to start digging
and buries the ball along with himself and the female to a depth
of several feet, safe from competition, predation, parasitism, and
adverse climatic conditions above ground. The male and female
copulate and she lays eggs, which feed on the dung (“coprophagy,”
meaning “feeding on feces”). In some species the pair remains
together to care for the brood. Among beetles they are rare in
the extent of their parental investment. When dung beetles are
killed by the antiparasitic drug ivermectin administered to cattle,
dung accumulates to a thickness of a foot or more on the African
savanna.
Spotted hyenas (Crocuta crocuta) in East Africa have a
unique mating system that has prompted outrageous and comical speculations in the past. Females are larger than males, and
the dominant “alpha” female has precedence at kills (along with
her offspring). Females have higher circulating androgen levels
than males, which may explain their size and tendency to be
more aggressive. The clitoris is greatly enlarged and resembles a
penis, to such a degree that researchers have trouble distinguishing males from females. The vagina and urogenital canal of the
female pass through the clitoris, as in no other known mammal
(Figure 15). The clitoris must expand to allow a 4-pound fetus
to pass through. Dystocia (obstructed labor) has been observed
in captivity and has resulted in the death of many primiparous
females, and in those that survive, the fetus often suffocates during the prolonged passage.
How could such a dangerous anatomy evolve, seemingly at
the edge of survivability? One hypothesis, difficult to test, states
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Figure 15. The reproductive tract of the spotted hyena, an African carnivore, is
unique in all the world and is outrageous in its risk factors. The fetus (shown)
must pass through a tract which turns at almost 180 degrees and continues
through the canal of the enlarged clitoris. The clitoris, a homolog of the penis, is
enlarged in female spotted hyenas because of high androgen levels, thought to
have evolved because they conferred survival benefits upon the female and her
young by increasing her body size and dominance at highly competitive feeding
opportunities at kills. The clitoris and penis look so much alike that experienced
researchers have trouble distinguishing males from females, except by adult size.
The vagina and urogenital canal of the female pass through the clitoris, as in no
other known mammal. Obstructed labor and suffocation result in the death of a
high percentage of neonates.
that under the conditions of competing for food at a kill, where a
clan of 30 or more adults and juveniles compete fiercely at a single
carcass on the East African savanna, mutations conferring greater
size and strength on a female would provide a survival advantage
for her and her offspring, and such genes would spread. Another
question remains: Why have high androgen levels not evolved
in females of other mammals?
The late Stephen Jay Gould argued that the male-mimicking
genitalia of female spotted hyenas are “spandrels,” or coincidental spin-offs, of high testosterone levels. In a famous paper coauthored with Richard C. Lewontin, Gould argued that many
traits of animals and plants did not arise as adaptations at all
but as by-products of other traits that were adaptive. He used
the term “spandrel” as a metaphor, comparing these traits to the
curved triangular spaces formed between the arches of the great
central dome of St. Mark’s Cathedral in Venice. Each spandrel
in the cathedral is elaborately decorated but is in essence a secondary by-product or “spin-off” of the vaulted arches supporting
the dome.
Gould reminds us that the mammalian penis and clitoris are
homologous pairs of organs, as are the scrotal sac and labia majora. In female spotted hyenas the clitoris and labia majora have
enlarged to resemble penis and scrotum, but only as “spandrels,”
not as adaptive organs used in social interactions, as the earlier
hyena researcher Hans Kruuk had proposed. Gould admitted that
his interpretation may not be the last word and that ongoing
research may eventually clarify the origins of the anatomy and
behavior of spotted hyenas (10).
Karen Blixen (Isak Dinesen) quoted a myth about spotted
hyenas in Out of Africa (1938):
JULY 2005
Figure 16. Naked mole-rats, which live underground in East Africa, are among the
most unusual mammals in the world, almost hairless and almost blind, with only
one reproductive female and several reproductive males. Other colony members
specialize in colony tasks and do not reproduce; the caste system has been compared
to eusocial insects, which also have nonreproductive workers. This small group of
nonreproductive workers was collected by a researcher in East Africa whom we
encountered on a dirt road, where he was capturing workers that appeared at the
surface while excavating cavity tunnels. They are caught by snakes in the same way,
as they emerge at the surface. A colony may comprise 80 individuals, or sometimes
up to several hundred, and feed on plant roots and tubers underground. This diet is
high in cellulose, which is difficult to digest. Their gut microbiota help with digestion,
and coprophagy (ingestion of feces) allows maximal extraction of nutrients.
All hyenas, you will know, are hermaphrodites, and in Africa . . .
on a full-moon night they will meet and join in a ring of copulation
wherein each individual takes the double part of male & female. . . .
Do you consider now . . . that it should be, on account of this fact,
harder to a hyena than to other animals to be shut up by itself in
a cage? Would he feel a double want, or is he, because he unites in
himself the complementary qualities of creation, satisfied in himself,
and in harmony? In other words, since we are all prisoners in life, are
we happier, or more miserable, the more talents we possess? (11)
Belief that spotted hyenas are hermaphrodites persists today in
parts of Africa.
Another remarkable East African carnivore, the dwarf mongoose, can be seen on any safari to the Serengeti Plains or Masai
Mara, living in abandoned termite mounds. Dwarf mongooses are
no larger than small squirrels, and their social system is extraordinary, with an alpha male and alpha female forming a lifelong
pair-bond. They dominate all other members and are likely to be
the parents of all young born in the pack. The alpha male drives
off any other male who attempts to mate with his partner. The
most striking feature of their social system is the rearing of young
by both related and unrelated individuals. Some pack members
have emigrated from other packs and are not related to the pack
members. Nevertheless, some of the unrelated females serve as
“wet nurses,” lactating and feeding the babies of the dominant
female!
The naked mole-rat has perhaps the most remarkable social
organization of all mammals, living underground in extensive colonies in East Africa. A caste system divides them up into specialized
morphotypes that perform specific functions, the closest that a
mammal society comes to a social insect colony (see discussion
under illustration, Figure 16). Workers excavating tunnels emerge
at the surface kicking out dirt, an activity dubbed “volcanoing,”
with their uplifted rear ends a tempting target for a snake or a
human researcher!
EVOLUTION OF SEXUALITY: BIOLOGY AND BEHAVIOR
251
Male African elephants have a unique male mating strategy
called “musth,” in which males come into a sexually active estruslike state unknown in other mammals. Their serum testosterone
levels and aggressive behavior both rise markedly, and two males
who are simultaneously in musth may inflict serious injuries on
each other. Perhaps for this reason, in one study population the
males were found to “straddle” the times of the year when they
came into musth. Elephants have a very close and personal
family life, which has been severely disrupted by poaching and
capture of juveniles. When an elephant family is gunned down
and the juveniles captured, those same juveniles often show seriously disturbed behavior as adolescents, resembling posttraumatic
stress disorder in humans, with murderous aggression on other
animals (12).
Bonobos (close relatives of chimpanzees, the other great ape
most closely related to us) engage in “recreational” sex as a daily
activity—females with females, males with males, and adults
with young. In anthropomorphic psychiatric jargon, this behavior might be called “polymorphous perverse,” even though it is
often initiated by the juveniles! It is seen in both wild and captive
bonobos; one zookeeper told me she had to explain this behavior
daily to visitors, with some embarrassment. Females engage in
frontal “genital-genital rubbing” and seem to become excited as
they do. Males usually do not ejaculate during recreational sex. In
a behavior dubbed “penis-fencing,” two males hang face to face
from a branch while rubbing their erect penises together. Bonobo
behavior resembles that proposed for early humans in three ways:
females are sexually receptive for long periods; sexual life is rich
and serves purposes other than reproduction; and bonobos walk
bipedally with ease much of the time. Frans de Waal, the primate
researcher who in all the world may know as much about chimpanzees and bonobos as Jane Goodall, has studied their behavior
in captivity for decades at the Yerkes Primate Research Center
in Georgia and has written extensively on their complex social
interactions.
The above examples of reproductive strategies in animals
and plants are a small sample of the endless varieties, known and
unknown. How do we make sense of the jungle of variations?
HYPOTHESES FOR THE PREVALENCE OF SEXUAL REPRODUCTION
Why is sexual reproduction almost universal in eukaryotes
(animals, plants, fungi, protists)? Reproduction per se doesn’t
require sex, and sex is expensive: only one half of an individual’s
genes are passed on to each offspring, and courtship and mating
are risky and energetically costly.
Over a dozen hypotheses attempt to explain the overwhelming prevalence of sexuality over asexuality. The two that are supported by the most evidence are 1) the host-parasite (pathogen)
arms race (Red Queen hypothesis) and 2) the purging of the
genome of deleterious mutations.
The Red Queen hypothesis is described in more detail in
my paper in BUMC Proceedings (13) and in great detail in Matt
Ridley’s book, The Red Queen (14). This hypothesis states that
in a world of dynamically changing biotic and abiotic environments, different lottery tickets (different genotypes created by
sexual reproduction) provide a hedge against loss of all of one’s
offspring to pathogens, parasites, predators, or harsh environmental conditions. Support for this hypothesis comes from the
252
fact that pathogens and parasites are best adapted to defeat the
most common host genotypes (uncommon genotypes have an
advantage) and from the extraordinary diversity of major histocompatibility complex (MHC) genes, which code for proteins
involved in recognition of pathogens and transport of protein
fragments to the cell surface for recognition by T cells of the
immune system. Some MHC genes have over 100 alleles in the
population of a species, maintained by selection; this number of
alleles is unheard of for other genes.
To understand the second hypothesis for the ubiquity of sex,
which is called “Muller’s ratchet,” consider photocopying a document, then copying the copy, and repeating this process again and
again. Each copy becomes more degraded than the last. This is
what happens in asexual reproduction, with an organism cloning
itself again and again, each time accumulating more mutations,
ratcheting down the quality. DNA repair mechanisms correct
some of those mutations, but not all. In sexual reproduction,
the crossing-over of chromosome segments in meiosis allows
for greater error correction, as there is a template on the other
chromosome. In addition, with the reshuffling of genes in sexual
reproduction, you can imagine a bell curve of individuals in the
population, with one end of the curve harboring members with
the most mutations and the other end having those with the
fewest mutations. Those at the end with more mutations will
have lower reproductive success than those at the other, thereby
purging the gene pool of many harmful mutations. The advantage
of this distribution is summed up by George Bernard Shaw’s reply
to the actress who suggested that they have a child together,
which would have her beauty and his brains: “Yes, madam, but
what if it had my beauty and your brains?” (the wrong end of
the bell curve).
The privilege of purging mutations by means of a bell curve
(Muller’s ratchet) is denied an asexual organism. It may be a
valid explanation for sexuality, but it does not rule out the Red
Queen hypothesis. Both may contribute to the benefits of sexual
reproduction.
The bottom line is that we do not know why sexuality is
the winning strategy, by a wide margin. Can we learn from the
examples when it is not?
ASEXUALITY
Some invertebrates reproduce sexually when the environment
turns nasty, as with abrupt parasite infestation or the drying up
of their habitat. This gives them the advantage of a diversity
of genotypes in their progeny, some of which may survive the
environmental change. During favorable environmental conditions, these invertebrates choose asexual reproduction, cloning
the genotype that worked well under those conditions. They
therefore have the best of both worlds, sexual and asexual.
Other rare invertebrates are exclusively asexual. Bdelloid rotifers, tiny aquatic invertebrates that have lived and thrived for
40 million years without sex, are “something of an evolutionary
scandal,” according to the late John Maynard Smith, who studied
the evolution of sexuality for most of his life. These rotifers have
flagrantly falsified the hypothesis that asexual organisms should
become extinct in a relatively short time because of accumulation
of harmful mutations in nonrecombining genomes. Males are
unknown in these little animals, which are found in fresh water
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and moist habitats worldwide. A study of their DNA suggests that
their genome “froze” millions of years ago, when meiosis ceased
and they became asexual.
One such rotifer is named Philodina roseola. The biologist
Olivia Judson, in Dr. Tatiana’s Sex Advice to All Creation, quoted
Miss Philodina, who explained the “scandalous” longevity of
her kind:
We bdelloids travel in both space and time. Of course, we can’t travel
backward in time: nobody can do that. But we can go forward. We
have a trick called anhydrobiosis. It’s a state of suspended animation.
Essentially, we dry up and blow away. . . . It’s risky. Anhydrobiosis
is difficult. . . . Many bdelloids never recover. But if you do survive,
you come back to life in a new place and time, healthier and happier than before (8).
Another case of long-lasting asexuality is that of mycorrhizal
fungi, which collaborate with flowering plants in an ancient and
widespread mutualism. The fungal filaments invade plant roots
and provide the plants with minerals from the soil, in turn receiving carbohydrates from the plant (products of photosynthesis,
unknown in fungi). Like bdelloid rotifers, these fungi have been
asexual for millions of years. But there is a catch: their cells
contain hundreds of nuclei, and a recent study found that each
nucleus contains many different sequences of the same genes for
ribosomal DNA. This may be a unique kind of sexuality that
protects this ancient lineage from accumulating harmful mutations over time.
A small number of asexual, parthenogenetic salamanders in
North America have persisted for millions of years (15). These
lineages are all-female but require sperm from males of a different, sexual species to initiate egg division and embryogenesis.
Fertilization does not occur, so the male’s genes are wasted. Why
should males of a sexual species waste their time and sperm in
such a manner? Why should genes promoting that behavior
persist? The answer, at least in one case, seems to be that the
males become more attractive to females of their own species if
they are observed consorting with females of the other species.
Females of both species look alike, and those of the sexual species may mistakenly identify the other females as some of their
own. Female choice may thus maintain the behavior (16), as
long as the parthenogenetic females mimic the appearance of
the sexual females.
Only lizards, among vertebrates, have fully parthenogenetic
species, with no need for stimulation of egg development by sperm
from a male of another species. These lizards have fully parthenogenetic populations able to reproduce without males. Some tropical lizards have both sexual and parthenogenetic populations;
with habitat disturbance, only one parthenogenetic female need
find her way into a favorable habitat to found a new colony, which
can outproduce the bisexuals in a short time. Her offspring are
identical copies of herself and so can reproduce without mating,
twice as fast as a sexual colony. Parthenogenesis may survive as
a viable strategy because of this sporadic advantage.
A study published in 2005 found that the favorite laboratory
plant Arabidopsis can repair damaged genes and restore normal
floral morphology without the help of the template of a second
normal copy of the damaged gene (17). This is an unprecedented
finding with no known explanation, and if it is found to be more
widespread it may help explain the occasional evolutionary lonJULY 2005
gevity of asexual species such as bdelloid rotifers. One suggestion
is that there may be an RNA “backup copy” of the entire genome
that has been entirely undetected and can act as a template.
Computer metaphors in biology are multiplying like rabbits!
BACTERIALLY INDUCED “ASEXUALITY” IN ARTHROPOD HOSTS
Sexuality may be ubiquitous because of infectious and parasitic diseases, but there are specialized bacteria that may literally
eliminate sexuality in their host. The tiny bacterium Wolbachia
spends its entire life within the ovaries and testes of many insects
and is transmitted from female to offspring through the egg’s cytoplasm (18). Because sperm are almost empty of cytoplasm, males
are usually unable to pass on the bacterium. That fact provides a
clue to the bacterium’s strategy: eliminate males, or at least reduce
them to insignificance, because the bacterium’s genes are spread
only by females. The result is a skewed sex ratio with few males,
and in some cases loss of all males, with resulting parthenogenesis.
We once thought this was an evolved trait of the host species,
but now it emerges as a takeover by Wolbachia.
Some wasp species that are hosts of Wolbachia become parthenogenetic for as many generations as the bacterium is there.
Asexuality can be “cured” by treating the wasps with antibiotics
or subjecting them to heat in the laboratory, either of which kills
the bacteria. Males reappear among the offspring. If the antibiotic
is continued over several generations, the population becomes
permanently sexual and does not revert after cessation of treatment, unless it becomes reinfected in the wild.
How common is Wolbachia infection? It occurs in members
of over 90% of arthropod species, including 5 orders of insects,
an isopod, and a spider mite. In most cases a skewed sex ratio,
not asexual reproduction, results. Wolbachia is only one of many
male-killing bacteria that are common in insects (19).
Wolbachia may soon become more newsworthy, as they are
essential symbionts of the major pathogenic filarial nematode
parasites of humans, including Onchocerca volvulus, which causes
river blindness. Antimicrobials that kill the Wolbachia symbionts
also kill the nematode hosts and may become useful in treating
the debilitating diseases caused by the nematodes (20, 21).
ARE BACTERIA AND VIRUSES ASEXUAL?
Although bacteria and archaebacteria replicate asexually, and
viruses are cloned asexually by their host cell, rampant horizontal gene transfer (from one cell to another, not from parent to
offspring) also shapes their genomes. In bacteria we see plasmidmediated transfer of genes that confer antibiotic resistance and
virulence, and in the influenza A virus we see mixing of genes
and gene segments when both an avian and a mammalian strain
infect an intermediate mammal host simultaneously, such as
pigs in southeast Asia, where ducks, swine, and humans have
regular and intimate contact. Such mixing of genes in bacteria
and viruses, called “parasexuality,” is as effective as any form of
sexual reproduction in generating genotypic diversity and can
occur instantaneously, not having to wait for a new generation of
progeny. Microbes enjoy much more rapid evolution and adaptation than their larger hosts.
We once thought the “tree of life” could be traced back to
an Ur-organism that would represent the earliest life form. The
biologist Carl Woese laid this idea to rest by proposing that the
EVOLUTION OF SEXUALITY: BIOLOGY AND BEHAVIOR
253
earliest life forms engaged in a promiscuous horizontal exchange
of genes, so that the trunk of the tree of life was actually a soup
of genes traded freely by primitive microbes.
CONFLICT BETWEEN THE SEXES: IMPRINTING
We should always ask: How do alleles get themselves better
represented in future generations, and do they do this by different
strategies in the two sexes?
There is no teleology here; natural and sexual selection act
by the logic of what works best. The use of words like “strategy”
is only a convenient anthropomorphic way to describe what
works best. We could avoid such words, but the alternative is
a cumbersome description such as, “Behavioral predispositions
have evolved in the competitive setting of specific variables.”
Nevertheless, there is an ongoing debate about whether to use
such anthropocentric descriptions. I favor their use for the sake
of simplicity and economy of expression, as long as we understand
what we are doing.
Strategies of courtship and mating should, by evolutionary
logic, be different for the sexes, which sometimes seem to be from
different planets. They obviously need each other, but they do
not have the same priorities. Anthropologist Meredith F. Small
has elegantly captured the essence of male-female reproductive
conflict:
Compelled by the urge to pass on genetic material to the next generation, the sexes must often cooperate in mating and parenting, but
each sex cooperates only under duress because females and males
operate under different reproductive rules set down in opposing
directions eons ago. Like an open wound that never heals, the conflict between males and females will never be resolved because the
evolutionary interests of the two sexes are forever locked in opposing
position. There is no right or wrong here, no sex better than the other,
just two types of individuals trying to win in the game of reproductive
success. The ground rules of the battle include cooperation, conflict,
and exploitation, and both sexes use these tactics equally (22).
Conflict between the sexes, at the most fundamental level,
takes the form of imprinting of DNA in egg and sperm. Imprinted
genes are epigenetically marked during gametogenesis so that they
are exclusively expressed in either egg or sperm genomes with
no change in their DNA sequence. A child’s genes are therefore
not all equal: in some cases, the copy from one parent is turned
off, and this affects the child’s ability to acquire resources in the
uterus and after birth. Imprinting may even last through life,
the alleles retaining a “memory” of their parental origin. There
is growing evidence that imprinting may contribute to disease
susceptibility, possibly by altering resource allocation to organs
over the course of a lifetime.
The asymmetry of interests of maternally and paternally inherited genes may take the form of differences in the placental
tissues interposed between mother and fetus. Gene knockout
experiments have shown that eliminating genes expressed from
sperm reduces the surface area for nutrient exchange, whereas
knocking out genes expressed in the egg increases the area for
exchange. The offshoot is that a shift toward greater nutrient
provisioning to the fetus is promoted by the father’s genes and
suppressed by those of the mother, both being compatible with
fetal life support but the one enhancing fetal survival and the
other preserving maternal resources for future reproductive op254
portunities (23). The conflict of the sexes is no more dramatically revealed.
Parthenogenesis does not occur in mammals, probably because there is only one parental genome (the maternal genome)
and some of the maternal gene copies are silenced by imprinting, with no unimprinted partner alleles to provide the critically
important gene products. Biparental reproduction is necessary
because of epigenetic modifications (such as imprinting) that
occur during gametogenesis. This results in unequal expression
of genes from parental chromosomes. In 2004 the first parthenogenetic mouse was artificially created in the laboratory and
developed to adulthood with the ability to reproduce normally
by mating with a male and delivering normal offspring (but was
only one of many that did not develop normally) (24). With a
stretch of the imagination and laboratory intervention, we can
finally propose that male mammals are unnecessary!
HOW MANY SEXES?
If you were a single-celled alga in a pond, you wouldn’t see
the world as splitting into males and females, argues a prominent sex researcher, Laurence Hurst of the University of Bath in
the United Kingdom. In some species of algae every member is
sexually equivalent. One slime mold has 13 gamete types, which
compete in a hierarchy, and somehow (for the time being), the
arrangement seems to be working. The biological diversity of
sexual reproduction has produced a different take on what sex
is. There is even an ant species believed to have a three-sex
system—a female and two types of males (25).
The bottom line is that we have adopted a stereotyped,
anthropomorphic view of sex. Some algae, fungi, and protists
dispense with a hard-and-fast division of sexes, and we can view
them as having multiple “sexes” or just mixing genes in any of a
myriad of ways, as bacteria and viruses do.
On the other hand, only two sexes—and two kinds of gametes—have evolved in the vast majority of eukaryotic organisms.
How would you answer your child’s question, “Why are there
two sexes?”
The simplest answer might start with the explanation that
gametes could be identical and still provide genetic diversity in
offspring. Gene reshuffling could occur even if sperm and egg
were identical (isogametes). So why are they different, with
eggs bloated with food resources and mitochondria, and sperm
consisting of anemic cytoplasm, a full complement of nuclear
genes, and a tail powered by a few mitochondria that aren’t allowed into the egg?
According to one model, one sex abandons its cytoplasm
and avoids conflict with mitochondria of the other sex. (Conflict
inevitably results when two entities interact in reproduction,
with natural selection weaning out the one or the other because
of small differences.) Sperm and egg diverged, so that each performed very different functions. The one provided resources in
the form of cytoplasmic food and mitochondria (and chloroplasts,
in plants); the other provided another set of genes, without mitochondria or chloroplasts to compete with those in the other
gamete. “Runaway” selection pushed each to its own extreme.
Although this is only one model, it is a popular one and
probably a good one for a tentative answer. Having two sexes
and two gamete types may be the best way to avoid conflict and
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VOLUME 18, NUMBER 3
get along. The result is a form of genomic conflict management,
important for organisms that reproduce by fusing two cells, bringing together both nuclear and cytoplasmic DNA. (The genome is
no longer the cooperative “republic of genes” it was once thought
to be.) The verdict: if you’re going to fuse, there should be different sexes, and if there are different sexes, the number should
usually be two.
sharks and eels! (One male Amazon River dolphin was even
observed to penetrate another’s blowhole!) Young male Masai
giraffes engage in long “necking” bouts, which seem to be a kind
of practice for later contests between adult males over access to
females (Figure 4). Young male sea lions also practice sparring
behavior (Figure 5). Males of almost any species of land vertebrate
mount other males, as juveniles and adults.
SEX DETERMINATION
Sex determination in animals is highly complex and poorly
understood. In mammals, males are the “heterogametic” sex (XY)
and females are “homogametic” (XX), but in birds and lepidopterans (butterflies and moths) it is just the opposite, females being
heterogametic and males homogametic.
In crocodilians (crocodiles, alligators, caimans, and gavials),
many turtles, and several lizards, sex assignment is by means of
temperature during embryogenesis. In the leopard gecko, an egg
incubation temperature of 26°C produces only females, 30°C
produces a female-biased sex ratio, 32.5°C results in a male-biased
ratio, and 34°C again produces almost all females (26). David
Crews, who has studied temperature-based sex determination
for decades at the University of Texas at Austin, believes that
incubation temperature has direct organizational effects on the
development of brain nuclei, notably in limbic structures such
as the hypothalamus. Phenotypic plasticity is abundantly in evidence in these reptiles. Sexual behavior, and not just gender, is
determined by temperature (27).
In a number of litter-bearing mammals such as mice, gerbils,
and rats, females sandwiched between two males in utero are less
attractive to males, have a masculinized anatomy, urine-mark
more often, and are more aggressive than females sandwiched
between two other females or between one female and one male.
The surge in testosterone levels in male fetuses diffuses through
the amniotic fluid, with higher concentrations reaching adjacent
fetuses. The opposite, feminizing effect is seen in males flanked
by females. Crews reminds us that sexuality is different from sex;
sexuality “goes beyond the components of sex and represents
the continuously variable suite of traits that emerge during the
organism’s lifetime, making each individual unique” (27).
Our stereotypical division of animals into male and female is
thus challenged. If we think of a continuum between male and
female, it appears that the reproductive tract and the central nervous system may end up at different points on the continuum.
The latest research—in its early stages—suggests that male
and female brains sometimes start down different developmental
paths from the outset, before hormones enter the picture; both
body and brain of a zebra finch were male on one side and female
on the other, hinting that more than sex hormones guided their
development (28).
“Homosexuality” in nonhuman animals has been disputed
endlessly with no meaningful conclusion, probably because the
term itself is anthropomorphic. In bonobos, as mentioned previously, brief “homosexual” pairings between either sex are common, but they occur along with heterosexual and adult-juvenile
pairings and are not long-term exclusive choices. Brief sexual
pairings between males of many animals are seen in nature and in
zoos; penguin males often engage in copulatory behavior together,
and male dolphins have paired with other males and with turtles
X AND Y CHROMOSOMES
Female mammals inherit an X chromosome from each parent,
whereas males inherit a single maternal copy. The mammalian
X and Y chromosomes are believed to have evolved from one
pair of autosomes (i.e., all the other chromosomes) within the
last 300 million years, when one member of the pair acquired
a male-determining locus. Male-advantage alleles accumulated
on the proto-Y, and the combination was preserved by cessation
of recombination between the X and Y during meiosis in males,
except for a small “pseudoautosomal” region on the tip of the X
that recombines with equivalent segments on the Y. This opened
the door to a progressive degeneration of the Y as it accumulated
mutations, deletions, and repetitive elements that could not be
eliminated by DNA repair during meiosis. An X chromosome
spends two thirds of its time in a woman, where it can recombine
with another X, dodging the Muller’s ratchet that has so eroded
the Y. Some genes on the Y have been found to recombine with
palindromic copies in a hairpin-like fold, and this may serve to
repair some copying errors. But the decay of the Y chromosome is
continuing; two groups of rodents have already lost their Y (29).
Jokes about males have taken full advantage of this degeneracy
(modified from Maureen Dowd, The New York Times): Why, oh
Y, are men so insecure? Not only are men dwindling away as their
Y chromosomes disintegrate, but now their Y chromosomes have
been found to have sex with themselves. Narcissistic to the core.
Better to be an X chromosome than an ex-chromosome.
In female mammals, the nucleus of somatic cells developed a
way to silence most of the genes on one or the other X chromosome in each cell, the choice being random from cell to cell (the
calico cat demonstrates this random pattern in its fur colors). This
silencing prevents a double dose of gene products in females.
Males pass their X chromosome to their daughters (XX) but
never to their sons (XY), whereas females pass their X chromosomes to daughters and sons with equal frequency. Male mammals
are vulnerable to genetic diseases that are much more rare in
females, because males have only one X chromosome. If a mutated
gene occurs on that X, there is no equivalent allele on the Y to
provide the proper code for the trait. Like autosomal single-gene
disorders, X-linked diseases can be either recessive or dominant.
X-linked recessive diseases include hemophilia and some forms
of muscular dystrophy. These diseases are much more common
in males than females because two copies of the mutant allele
are required for the disease to occur in females, while only one
copy is needed in males.
In 2005 the human X chromosome was sequenced (30) and
revealed a big surprise: some 15% of genes on the X are not silenced, thereby providing a double dose of those gene products
to females. Another 10% are sometimes silenced and sometimes
not. All together, human females have 15% to 25% more active
X genes than males, giving them more of those gene products and
JULY 2005
EVOLUTION OF SEXUALITY: BIOLOGY AND BEHAVIOR
255
in some cases different alleles. Human females may therefore have
greater genetic diversity than males, and the X chromosome is
the home of many genes for brain structures.
The sexes not only have different priorities but also are differently endowed genetically.
THREE “GREAT DIVIDES”
Sexual vs asexual reproduction is one “great divide” in reproductive biology. There are two others to consider: internal vs external
fertilization and parental investment (male vs female).
Eggs are fertilized internally in mammals and birds, and these
males are rarely absolutely certain of their paternity. “Sneaky
copulations” are implicated by DNA analysis in more and more
bird species that were thought to be monogamous. Sperm competition occurs in vertebrates and invertebrates across taxa, because
females are now known to be highly “promiscuous” (another
anthropomorphic term) in a majority of animal species. Sperm
wars are universal among males, except in rare truly monogamous
species and in seahorses and pipefishes, where the male fertilizes
the eggs in his pouch.
External fertilization usually enables males to be more certain
of their paternity than internal fertilization. When a female fish
deposits her eggs on the sea floor, a lucky male deposits his sperm
onto the egg mass and stays there to guard it from insemination by
other males and from predation. Genes promoting male parental
care are likely to be adaptive and selected for, as they promote
survival of his offspring. Male frogs ride on the backs of females
in order to deposit their sperm on the eggs the moment she lays
them (Figure 17). External fertilization changes the dynamic of
male parental care; the male is now more likely to spread his
genes if he provides parental care. The female may now be free
to desert the eggs after laying them.
Sperm competition occurs with internal or external fertilization. Female fish that release their eggs into the water invite sperm
competition from males who rush in to fertilize them. Male red
jungle fowl release more sperm in their ejaculate when they mate
with a new female (after repeated matings with the same female)
and also if they perceive a high level of competition with other
nearby males (31).
Parental investment, the third “great divide,” sets the stage for
which sex competes the most for access to the other. It is considered by many to be the single most important difference between
the sexes. The sex that invests the most in the next generation is
the “limiting resource.” Consider mammals: the female becomes
pregnant (with tremendous costs and risks), delivers the young
(with still more risks), nurses the young (expensive in terms of
effort and nutritional demands), and usually raises the young
by herself. She thus provides much greater parental investment
than the male, who has only to desert her after mating and seek
another mating opportunity. Female mammals are thus the limiting resource; that is, each female is competed for by more males
than each male is competed for by females. Females can thus be
more choosy than males, and there is less variance in female reproductive success than in male reproductive success: females enjoy
mating success with relatively little differences, but there is great
variation in male success (some males are highly successful and
others are total losers). Female choice is a powerful form of sexual
selection in animals.
256
Figure 17. Golden toads, this pair in amplexus in the cloud forest of Monteverde,
Costa Rica, have never been seen since 1989. The small and isolated populations,
which occupied only a few square miles of cloud forest, are now apparently extinct,
and their social behavior has never been studied in detail. Many biologists have
searched for them in vain. At large pools of rainwater in the rainy season, as many
as several hundred males were once seen at one time; for the lucky few who saw
them, the sight was unforgettable.
Parental investment is usually greater in females than in males
in animals with internal fertilization. This is why in mammals
and birds we usually see greater competition among males for
access to females, rather than the other way around. Females are
usually the limiting resource. The rare exceptions are instructive:
consider phalaropes (shorebirds) and seahorses.
The three species of phalaropes in North America show
“reversed sexual dimorphism,” the females being larger and
more brightly colored than the males. The female competes aggressively with other females for mates. She abandons her eggs
after laying them, and the male incubates them and raises the
young by himself. This is a rare case of polyandry (“many males,”
in which females compete for mating with males), and begs an
explanation. One hypothesis: males can be counted on to rear
the young and females can increase their mating opportunities
by deserting; paternal investment is relatively large. But the real
question is, How did this strategy arise in phalaropes when it is
so rare elsewhere? And why is it rare?
The second instructive example of sex role reversal is that of
seahorses and pipefishes, in the family Syngnathidae (collectively
called syngnathids). As I mentioned, males of these fishes have
a specialized egg-brooding structure on the abdomen or tail into
(or onto) which females deposit their eggs. This arrangement
assures the male of his paternity, as he inseminates the eggs in
his own pouch or on his own tail. As with phalaropes, paternal
investment is high. The most complex pouches of seahorses have
placenta-like tissues that provide nourishment and oxygen to the
young. The chemical composition of the pouch fluid changes from
that of body fluids to that of seawater as “pregnancy” progresses.
Males protect, nourish, and oxygenate the developing embryos
for several weeks and then release them into the water as independent young. “Labor” may last hours or days.
Many seahorse species with complex brood pouches are
monogamous, and females of these species are busy guarding
their mate from other females. In other seahorse and pipefish
species, both males and females are polygamous, and both have
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VOLUME 18, NUMBER 3
multiple mating partners. In these polygamous species, it is often
the female who seeks more than one partner (polyandry); some
of these latter females are vividly colored, unlike the males, and
compete with other females for access to males.
Sex role reversal may thus occur as in phalaropes, but mostly
in nonmonogamous pairs. Mating habits may thus influence sex
roles just as parental investment does. Some seahorse males may
compete strongly with other males, and in these cases sex role
reversal is absent, except for carrying the young. Sexual selection
in syngnathids needs more study, as it is diverse and may provide
a wealth of insight into how mating strategies evolve (32, 33).
SUMMARY
This review of sexuality has several important messages:
• Sexual reproduction is far more common than asexual reproduction in plants and animals.
• Hypotheses for the prevalence of sexuality include the hostparasite and host-pathogen arms race and the purging of the
genome of deleterious mutations.
• Sexual selection is distinct from natural selection and is a key
player in evolution.
• Courtship and mating strategies are almost infinitely variable.
• Conflict between the sexes occurs at all levels, from mating
strategies to imprinting of genes.
• Parental investment may be the most important difference
between the sexes.
• In most animals with internal fertilization, females provide
more parental investment and are the “limiting resource.”
• When females invest more, they are the choosier sex and
there is more overt male-male competition for access to mates,
resulting in variance in reproductive success (with a more
even distribution of success in females).
• Alleles move into the future according to evolutionary logic,
which is usually different for the two sexes.
Some findings in this paper may change overnight, but the
lesson remains that evolutionary logic is important in the understanding of reproductive biology, at the level of genes, individuals,
and populations.
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